An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis

Abstract

The protozoan parasite Giardia intestinalis belongs to one of the earliest diverged eukaryotic lineages. This is also reflected in a simple intracellular organization, as Giardia lacks common subcellular compartments such as mitochondria, peroxisomes, and apparently also a Golgi apparatus. During encystation, developmentally regulated formation of large secretory compartments containing cyst wall material occurs. Despite the lack of any morphological similarities, these encystation-specific vesicles (ESVs) show several biochemical characteristics of maturing Golgi cisternae. Previous studies suggested that Golgi structure and function are induced only during encystation in Giardia, giving rise to the hypothesis that ESVs, as a Giardia Golgi equivalent, are generated de novo. Alternatively, ESV compartments could be built on the template structure of a cryptic Golgi in trophozoites in response to ER export of cyst wall material during encystation. We addressed this question by defining the molecular framework of the Giardia secretory apparatus using a comparative genomic approach. Analysis of the corresponding transcriptome during growth and encystation revealed surprisingly little stage-specific regulation. A panel of antibodies was generated against selected marker proteins to investigate the developmental dynamics of the endomembrane system. We show evidence that Giardia accommodates the export of large amounts of cyst wall material through re-organization of membrane compartment(s) in trophozoites with biochemical similarities to ESVs. This suggests that ESVs are selectively stabilized Golgi-like compartments in a unique and archetypical secretory system, which arise from a structural template in trophozoites rather than being generated de novo.